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Sympetaly in Apiales (Apiaceae, Araliaceae, Pittosporaceae)

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Sympetaly in Apiales (Apiaceae, Araliaceae, Pittosporaceae) South African Journal of Botany 2004, 70(3): 458–467 Copyright © NISC Pty Ltd Printed in South Africa — All rights reserved SOUTH AFRICAN JOURNAL OF BOTANY ISSN 0254–6299 Sympetaly in Apiales (Apiaceae, Araliaceae, Pittosporaceae) C Erbar* and P Leins Heidelberg Institute of Plant Sciences (HIP) — Biodiversity and Plant Systematics, University of Heidelberg, Im Neuenheimer Feld 345, D-69120 Heidelberg, Germany * Corresponding author, e-mail: [email protected] Received 10 March 2003, accepted in revised form 24 October 2003 In all recent molecular sequence based analyses Pittosporum) the corollas are initiated from a continu- Apiales come out to be placed within a broadly defined ous ring primordium corresponding exactly to the group Asteridae. Within ‘euasterids II’ Apiales development in Campanulales–Asterales and (Apiaceae, Araliaceae, Pittosporaceae, Aralidiaceae, as Dipsacales. Only in Pittosporaceae further growth of well as some former cornaceous taxa) form a mono- this primordium results in a weak sympetaly in adult phyletic group in a position close to Asterales– flowers. Molecular data suggest that the subfamily Campanulales and Dipsacales. Also from a floral devel- Hydrocotyloideae is polyphyletic, with Hydrocotyle opmental point of view the mostly choripetalous Apiales belonging to the lineage not placed within Apiaceae but are not out of place among these sympetalous orders: more closely related to Araliaceae, a position fitting well In members of Apiales (Apiaceae: Hydrocotyle; with the mode of formation of the corolla. Araliaceae: Aralia, Hedera; Pittosporaceae: Sollya, Introduction Flowers with a corolla tube can be found in many members tube formation, a corolla tube ontogenetically can be initiat- of the angiosperms, but are concentrated in the upper evo- ed extremely early, namely before the petal primordia arise. lutionary level. The combination of the character ‘sympetaly’ The Compositae are a good example of this mode of corol- with the character ‘one stamen whorl alternate with the la tube inception, which is called ‘early sympetaly’: The corolla-lobes and isomerous, or stamens fewer than the enlargement of an initially hemispherical floral apex into a corolla-lobes’ circumscribes a group which was established plug stage and subsequent funnel stage is due to a ring as the subclass ‘Asteridae’ by Takhtajan in 1964. Cronquist meristem (periclinal cell divisions below the dermatogen in maintained the subclass in all his later classifications (e.g. the periphery of the floral primordium). Later on five corolla Cronquist 1981). The group is also characterised by lobes arise on this ring meristem or ring primordium. The unitegmic and tenuinucellate ovules. stamen primordia are initiated alternating with the petal pri- All corolla tubes were assumed to be structurally homolo- mordia and internal to the interprimordial petal areas — the gous and their formation has been regarded as a typical petal primordia appear to be connected by flat shoulders. example of a ‘congenital fusion’ of adjacent organs. Further continuous enlargement of the former ring primordi- Ontogenetical studies, however, have shown that sym- um results in the corolla tube (see e.g. Figures 2–4 in Erbar petalous corollas s. str.1 can be formed in several ways, par- 1991, Figures 80–81 in Erbar and Leins 1996, Figure 40 in ticularly as regards the timing of their initiation. Thus a Leins 2000). Early sympetaly, i.e. the occurrence of an broadly used term ‘congenital fusion’ refers to rather diverse early corolla ring primordium, is also found in all members ontogenetical modes of growth. of the Campanulales s.l. (Brunoniaceae, Calyceraceae, The mode of development, in which the corolla lobes are Campanulaceae, Goodeniaceae, Lobeliaceae, initiated as separate primordia and become connected only Menyanthaceae, Sphenocleaceae, Stylidiaceae) investigat- later on, is called ‘late sympetaly’ (see Erbar 1991, Erbar ed until now. In these families a corolla ring primordium is and Leins 1996). We can find either the formation of a bridge formed inside or above a calyx. Apart from the connecting more or less abruptly the initially free petals or Campanulales–Asterales-complex, early sympetaly seems successive steps of a relatively slow lateral extension of the to be present as a constant character in the Rubiales, petal bases (see Figures in Erbar 1991, Erbar and Leins Oleales and Dipsacales (Erbar 1991, Erbar and Leins 1996). 1996, Leins 2000). In both cases equal growth in the petal A few cases must be regarded as ‘transitional between bases and interprimordial regions results in the formation of early and late sympetaly’. In Apocynaceae (Asclepiadoideae), the corolla tube s. str. Different from this mode of corolla for example, five petal primordia arise on the rim of a plateau, South African Journal of Botany 2004, 70: 458–467 459 and the extension and connection of the petal bases coincide only flat shoulders remain after the inception of five stamens with the initiation of the stamen primordia. (Figure 3d). The adult flowers apparently are choripetalous Based upon extensive ontogenetical investigations and in (see Erbar and Leins 1985, Erbar 1988). comparison with other characters the developmentally differ- entiated character states ‘early’ or ‘late sympetaly’ proved to Sympetaly in Apiaceae be good markers for systematic considerations and we recognise two blocks of orders within the Asteridae and relat- No indication of early sympetaly was seen in Saniculoideae ed groups (Erbar and Leins 1996). To a certain degree the (see Figures 1, 3–4 for Eryngium campestre, Sanicula two groups correspond with the presence or absence of europaea and Astrantia major in Leins and Erbar (2004)) or in chemical compounds, namely iridoid compounds and poly- Apioideae (see Figures 5, 7 for Foeniculum vulgare and acetylenes (see Erbar 1991). A much better correlation in the Levisticum officinale in Leins and Erbar (2004)). bipartition of the Asteridae results, if we transpose our char- acter states on the cladogram from Chase et al. (1993) based Sympetaly in Pittosporaceae on rbcL sequence investigations. Our Asteridae A-block — dominated by ‘late sympetaly’ — corresponds nearly exactly In Pittosporum tobira (Erbar and Leins 1995) the petal pri- with the asterid I-clade and our Asteridae B-block — charac- mordia are joined laterally at the time of initiation (Figures terised by ‘early sympetaly’ throughout — with the asterid II- 4a–b). Sympetaly is expressed very weakly in older flower clade (see Figures 11–12 in Leins and Erbar 1997). buds (arrow in Figure 4f) or in adult flowers. Sometimes a In the last few years the taxon ‘subclass Asteridae sensu distinct corolla tube is simulated by interlocking of the epi- Cronquist’ has been abandoned. Due to cladistic analyses of dermal cells of the adjacent free corolla lobes, but this is molecular data only expanded Asteridae (in a broad sense) unrelated to a true corolla tube whose initiation we are are regarded as monophyletic. Broadly circumscribed presently considering. In Pittosporum as well as in Sollya a Asterids contain some formerly dilleniid or rosid taxa like true corolla tube is restricted to the very base. Nevertheless, Ericales (including Primulaceae), Cornales and Apiales in Sollya fusiformis (Erbar and Leins 1996) ‘early sympetaly’ (Chase et al. 1993, Olmstead et al. 1993, Plunkett et al. is distinctly expressed during early development by initiation 1996a, APG 1998, Soltis et al. 1997, 2000, Savolainen et al. of a flat ring primordium (Figure 5a), on which five petal pri- 2000). mordia differentiate (Figure 5b). As in Pittosporum (Figures The two groups Cornales and Apiales are of particular inter- 4d–e), the stamen primordia arise clearly internal to the est because they have tetracyclic flowers throughout, but in interprimordial petal areas (Figure 5c). adult flowers the corolla is mostly choripetalous. Traditionally Araliaceae and Apiaceae have been placed in the Apiales. Discussion Molecular data (e.g. Olmstead et al. 1992, 1993, Plunkett et al. 1992, 1996a, Chase et al. 1993, Savolainen et al. 2000, Systematic position of Apiales Soltis et al. 2000, Plunkett 2001) also support a close rela- tionship of Pittosporaceae to the latter two families. From the floral developmental point of view the Apiales fit well in the early sympetalous asterid II-group where they, Sympetaly in Araliaceae based on molecular data, come out as sister to the Asterales (see e.g. Plunkett et al. 1996a, Savolainen et al. 2000, Soltis In the Araliaceae the corolla is initiated as a low ring pri- et al. 2000). The connection Apiales–Asterales, however, mordium which does not grow up forming a tube, so that the has already been noted because of similarities in secondary petals are free from each other in the adult flower (Erbar and chemistry (Hegnauer 1971, 1990) and in morphology (see Leins 1988). In Hedera helix, the initiation of the low corolla Leins and Erbar 1987, Erbar 1988, Erbar and Leins 1988, ring primordium takes place nearly simultaneously with the 1995). Systematically relevant characters are: formation of the petal primordia (Figure 1). As in Aralia elata • ethereal oils (Figure 2) the circular corolla primordium is inside the calyx. • polyacetylenes (falcarinone type) (Hegnauer 1989, 1990, Although in Aralia the ring primordium is somewhat more Frohne and Jensen 1992) pronounced (Figure 2e), in Aralia and Hedera, the stamen • anthraquinones (acetate-derived) (Jensen 1992) primordia originate distinctly
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